Ionizing radiation-induced expression of INK4a/ARF in murine bone marrow-derived stromal cell populations interferes with bone marrow homeostasis.
Abstract
Alterations of the BM microenvironment have been shown to occur after chemoradiotherapy, during aging, and after genetic manipulations of telomere length. Nevertheless, whether BM stromal cells adopt senescent features in response to these events is unknown. In the present study, we provide evidence that exposure to ionizing radiation (IR) leads murine stromal BM cells to express senescence markers, namely senescence-associated β-galactosidase and increased p16(INK4a)/p19(ARF) expression. Long (8 weeks) after exposure of mice to IR, we observed a reduction in the number of stromal cells derived from BM aspirates, an effect that we found to be absent in irradiated Ink4a/arf-knockout mice and to be mostly independent of the CFU potential of the stroma. Such a reduction in the number of BM stromal cells was specific, because stromal cells isolated from collagenase-treated bones were not reduced after IR. Surprisingly, we found that exposure to IR leads to a cellular nonautonomous and Ink4a/arf-dependent effect on lymphopoiesis. Overall, our results reveal the distinct sensitivity of BM stromal cell populations to IR and suggest that long-term residual damage to the BM microenvironment can influence hematopoiesis in an Ink4a/arf-dependent manner.
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Damage to the HSC niche, such as induction of BM stromal cell senescence, plays a role in IR-induced residual BM injury.
“damage to the HSC niche, such as induction of BM stromal cell senescence, and a negative bystander effect of TBI on HSCs, also play a role in IR-induced residual BM injury.32,33”
From Total body irradiation causes long-term mouse BM injury via induction of HSC premature senescence in an Ink4a- and Arf-independent manner (2014) · cites this paper as [32]
IR induced senescence in BM stromal cells in a p16- and Arf-dependent manner.
“IR induced senescence in BM stromal cells in a p16- and Arf-dependent manner.32”
From Total body irradiation causes long-term mouse BM injury via induction of HSC premature senescence in an Ink4a- and Arf-independent manner (2014) · cites this paper as [32]
Cites
1 retracted
Systemic signals regulate ageing and rejuvenation of blood stem cell niches
Mayack, S. R., Shadrach, J. L., Kim, F. S., & Wagers, A. J. (2010) · Nature · doi:10.1038/nature08749 · Cited by 135 · see citing works
RetractedA biomarker that identifies senescent human cells in culture and in aging skin in vivo.
Dimri, G. P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E. E., Linskens, M., Rubelj, I., & Pereira-Smith, O. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.20.9363 · Cited by 7,477 · see citing works
CDK inhibitors: positive and negative regulators of G1-phase progression
Sherr, C. J., & Roberts, J. M. (1999) · Genes & Development · doi:10.1101/gad.13.12.1501 · Cited by 6,115 · see citing works
Cellular senescence: when bad things happen to good cells
Campisi, J., & d'Adda di Fagagna, F. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2233 · Cited by 4,441 · see citing works
Chronic Health Conditions in Adult Survivors of Childhood Cancer
Oeffinger, K. C., Mertens, A. C., Sklar, C. A., Kawashima, T. I., Hudson, M. M., Meadows, A. T., Friedman, D. L., Marina, N. M., Hobbie, W. L., Kadan‐Lottick, N. S., et al. (2006) · New England Journal of Medicine · doi:10.1056/nejmsa060185 · Cited by 3,597 · see citing works
Osteoblastic cells regulate the haematopoietic stem cell niche
Calvi, L. M., Adams, G. B., Weibrecht, K. W., Weber, J. M., Olson, D. P., Knight, M. C., Martin, R. P., Schipani, E., Pajevic, P. D., Bringhurst, F. R., et al. (2003) · Nature · doi:10.1038/nature02040 · Cited by 3,433 · see citing works
Mesenchymal and haematopoietic stem cells form a unique bone marrow niche
Méndez‐Ferrer, S., Michurina, T. V., Ferraro, F., Mazloom, A. R., MacArthur, B. D., Lira, S. A., Scadden, D. T., Ma’ayan, A., Enikolopov, G., & Frenette, P. S. (2010) · Nature · doi:10.1038/nature09262 · Cited by 3,381 · see citing works
A DNA damage checkpoint response in telomere-initiated senescence
Fagagna, F. D. D., Reaper, P. M., Clay-Farrace, L., Fiegler, H., Carr, P., von Zglinicki, T., Saretzki, G., Carter, N. P., & Jackson, S. P. (2003) · Nature · doi:10.1038/nature02118 · Cited by 2,855 · see citing works
Identification of Clonogenic Common Lymphoid Progenitors in Mouse Bone Marrow
Kondo, M., Weissman, I. L., & Akashi, K. (1997) · Cell · doi:10.1016/s0092-8674(00)80453-5 · Cited by 2,253 · see citing works
BRAFE600-associated senescence-like cell cycle arrest of human naevi
Michaloglou, C., Vredeveld, L. C. W., Soengas, M. S., Denoyelle, C., Kuilman, T., van der Horst, C. M. A. M., Majoor, D. M., Shay, J. W., Mooi, W. J., & Peeper, D. S. (2005) · Nature · doi:10.1038/nature03890 · Cited by 2,160 · see citing works
Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints
Bartkova, J., Rezaei, N., Liontos, M., Karakaidos, P., Kletsas, D., Issaeva, N., Vassiliou, L.-V. F., Kolettas, E., Niforou, K., Zoumpourlis, V. C., et al. (2006) · Nature · doi:10.1038/nature05268 · Cited by 1,986 · see citing works
Pomerantz, J., Schreiber-Agus, N., Liégeois, N. J., Silverman, A., Alland, L., Chin, L., Potes, J., Chen, K., Orlow, I., Lee, H.-W., et al. (1998) · Cell · doi:10.1016/s0092-8674(00)81400-2 · Cited by 1,521 · see citing works
Ink4a/Arf expression is a biomarker of aging
Krishnamurthy, J., Torrice, C., Ramsey, M. R., Kovalev, G. I., Al-Regaiey, K., Su, L., & Sharpless, N. E. (2004) · Journal of Clinical Investigation · doi:10.1172/jci22475 · Cited by 1,486 · see citing works
Senescence in premalignant tumours
Collado, M., Gil, J., Efeyan, A., Guerra, C., Schuhmacher, A. J., Barradas, M., Benguría, A., Zaballos, A., Flores, J. M., Barbacid, M., et al. (2005) · Nature · doi:10.1038/436642a · Cited by 1,482 · see citing works
Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a
Janzen, V., Forkert, R., Fleming, H. E., Saito, Y., Waring, M. T., Dombkowski, D. M., Cheng, T., DePinho, R. A., Sharpless, N. E., & Scadden, D. T. (2006) · Nature · doi:10.1038/nature05159 · Cited by 1,106 · see citing works
p16INK4a induces an age-dependent decline in islet regenerative potential
Krishnamurthy, J., Ramsey, M. R., Ligon, K. L., Torrice, C., Koh, A., Bonner-Weir, S., & Sharpless, N. E. (2006) · Nature · doi:10.1038/nature05092 · Cited by 1,003 · see citing works
Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing
Molofsky, A. V., Slutsky, S. G., Joseph, N. M., He, S., Pardal, R., Krishnamurthy, J., Sharpless, N. E., & Morrison, S. J. (2006) · Nature · doi:10.1038/nature05091 · Cited by 972 · see citing works
Medical Assessment of Adverse Health Outcomes in Long-term Survivors of Childhood Cancer
Geenen, M. M., Cardous-Ubbink, M. C., Kremer, L. C. M., van den Bos, C., van der Pal, H. J. H., Heinen, R. C., Jaspers, M., Koning, C. C. E., Oldenburger, F. R., Langeveld, N. E., et al. (2007) · JAMA · doi:10.1001/jama.297.24.2705 · Cited by 860 · see citing works
Morikawa, S., Mabuchi, Y., Kubota, Y., Nagai, Y., Niibe, K., Hiratsu, E., Suzuki, S., Miyauchi-Hara, C., Nagoshi, N., Sunabori, T., et al. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20091046 · Cited by 833 · see citing works
Age-Associated Characteristics of Murine Hematopoietic Stem Cells
Sudo, K., Ema, H., Morita, Y., & Nakauchi, H. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.9.1273 · Cited by 722 · see citing works
Rombouts, W. J. C., & Ploemacher, R. E. (2003) · Leukemia · doi:10.1038/sj.leu.2402763 · Cited by 580 · see citing works
p16 <sup>INK4A</sup> is a robust <i>in vivo</i> biomarker of cellular aging in human skin
Ressler, S., Bartkova, J., Niederegger, H., Bartek, J., Scharffetter‐Kochanek, K., Jansen‐Dürr, P., & Wlaschek, M. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00231.x · Cited by 557 · see citing works
Robles, S. J., & Adami, G. R. (1998) · Oncogene · doi:10.1038/sj.onc.1201862 · Cited by 498 · see citing works
Noort, W. A., Kruisselbrink, A. B., Anker, P. S. I. `., Kruger, M., van Bezooijen, R. L., de Paus, R. A., Heemskerk, M. H. M., Löwik, C. W. G. M., Falkenburg, J. H. F., Willemze, R., et al. (2002) · Experimental Hematology · doi:10.1016/s0301-472x(02)00820-2 · Cited by 492 · see citing works
Cellular senescence in naevi and immortalisation in melanoma: a role for p16?
Gray-Schopfer, V. C., Cheong, S. C., Chong, H., Chow, J., Moss, T., Abdel-Malek, Z. A., Marais, R., Wynford-Thomas, D., & Bennett, D. C. (2006) · British Journal of Cancer · doi:10.1038/sj.bjc.6603283 · Cited by 394 · see citing works
Effects of aging on the homing and engraftment of murine hematopoietic stem and progenitor cells
Liang, Y., Zant, G. E. V., & Szilvassy, S. J. (2005) · Blood · doi:10.1182/blood-2004-11-4282 · Cited by 384 · see citing works
The pathological response to DNA damage does not contribute to p53-mediated tumour suppression
Christophorou, M. A., Ringshausen, I., Finch, A. J., Swigart, L. B., & Evan, G. I. (2006) · Nature · doi:10.1038/nature05077 · Cited by 382 · see citing works
Total body irradiation selectively induces murine hematopoietic stem cell senescence.
Wang, Y., Schulte, B. A., LaRue, A. C., Ogawa, M., & Zhou, D. (2006) · Blood · doi:10.1182/blood-2005-04-1418 · Cited by 351 · see citing works
Coppé, J.-P., Patil, C. K., Rodier, F., Sun, Y., Muñoz, D. P., Goldstein, J., Nelson, P. S., Desprez, P.-Y., & Campisi, J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060301 · Cited by 302 · see citing works
Ju, Z., Jiang, H., Jaworski, M., Rathinam, C., Gompf, A., Klein, C., Trumpp, A., & Rudolph, K. L. (2007) · Nature Medicine · doi:10.1038/nm1578 · Cited by 284 · see citing works
MacMillan, M. L., Blazar, B. R., DeFor, T. E., & Wagner, J. E. (2008) · Bone Marrow Transplantation · doi:10.1038/bmt.2008.348 · Cited by 276 · see citing works
Stromal damage as consequence of high-dose chemo/radiotherapy in bone marrow transplant recipients
Galotto, M., Berisso, G., Delfino, L., Podestà, M., Ottaggio, L., Dallorso, S., Dufour, C., Ferrara, G. B., Abbondandolo, A., Dini, G., et al. (1999) · Experimental Hematology · doi:10.1016/s0301-472x(99)00076-4 · Cited by 274 · see citing works
Harrison, D. E., Astle, C. M., & Delaittre, J. A. (1978) · The Journal of Experimental Medicine · doi:10.1084/jem.147.5.1526 · Cited by 228 · see citing works
Dominici, M., Rasini, V., Bussolari, R., Chen, X., Hofmann, T. J., Spano, C., Bernabei, D., Veronesi, E., Bertoni, F., Paolucci, P., et al. (2009) · Blood · doi:10.1182/blood-2008-10-183459 · Cited by 197 · see citing works
Meng, A., Wang, Y., Zant, G. E. V., & Zhou, D. (2003) · PubMed · Cited by 193 · see citing works
Le, O. N. L., Rodier, F., Fontaine, F., Coppe, J., Campisi, J., DeGregori, J., Laverdière, C., Kokta, V., Haddad, E., & Beauséjour, C. M. (2010) · Aging Cell · doi:10.1111/j.1474-9726.2010.00567.x · Cited by 168 · see citing works
Use of an alpha-smooth muscle actin GFP reporter to identify an osteoprogenitor population
Kalajzić, Ž., Li, H., Wang, L., Jiang, X., Lamothe, K., Adams, D. J., Aguila, H. L., Rowe, D. W., & Kalajzić, I. (2008) · Bone · doi:10.1016/j.bone.2008.04.023 · Cited by 167 · see citing works
Hong, E.-H., Lee, S., Kim, J., Lee, K.-H., Um, H., Kim, J., Kim, S. J., Kim, J., & Hwang, S. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.058628 · Cited by 159 · see citing works
Testa, N. G., Hendry, J. H., & Molineux, G. (1985) · PubMed · Cited by 141 · see citing works
SASPense and DDRama in cancer and ageing
Fumagalli, M., & di Fagagna, F. D. (2009) · Nature Cell Biology · doi:10.1038/ncb0809-921 · Cited by 103 · see citing works
Li, Y., Shi, C., Yuan, J., Yang, Y., Li, J., Ma, J., Wu, X., Freund, M., Pollok, K. E., Hanenberg, H., et al. (2009) · Blood · doi:10.1182/blood-2008-07-168138 · Cited by 66 · see citing works
Benabdallah, B., Allard, E., Yao, S., Friedman, G., Gregory, P. D., Eliopoulos, N., Fradette, J., Spees, J. L., Haddad, É., Holmes, M. C., et al. (2010) · Cytotherapy · doi:10.3109/14653240903583803 · Cited by 61 · see citing works
Masuda, S., Ageyama, N., Shibata, H., Obara, Y., Ikeda, T., Takeuchi, K., Ueda, Y., Ozawa, K., & Hanazono, Y. (2009) · Experimental Hematology · doi:10.1016/j.exphem.2009.07.008 · Cited by 47 · see citing works
Collis, S. J., Neutzel, S., Thompson, T. L., Swartz, M. J., Dillehay, L. E., Collector, M. I., Sharkis, S. J., & DeWeese, T. L. (2004) · Radiation Research · doi:10.1667/rr3197 · Cited by 22 · see citing works
Piersma, A. H., Brockbank, K. G. M., Ploemacher, R., & Ottenheim, C. P. E. (1985) · Transplantation · doi:10.1097/00007890-198508000-00018 · Cited by 12 · see citing works
Flagged first, then by citations
1 of the 46 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Clearance of senescent cells by ABT263 rejuvenates aged hematopoietic stem cells in mice
Chang, J., Wang, Y., Shao, L., Laberge, R.-M., Demaria, M., Campisi, J., Janakiraman, K., Sharpless, N. E., Ding, S., Feng, W., et al. (2016) · Nature Medicine · doi:10.1038/nm.4010 · Cited by 1,819 · see citing works
DNA damage checkpoints in stem cells, ageing and cancer
Sperka, T., Wang, J., & Rudolph, K. L. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3420 · Cited by 393 · see citing works
Hematopoietic Stem Cell Injury Induced by Ionizing Radiation
Shao, L., Luo, Y., & Zhou, D. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5635 · Cited by 337 · see citing works
Specification of haematopoietic stem cell fate via modulation of mitochondrial activity
Vannini, N., Girotra, M., Naveiras, O., Nikitin, G. F., Campos, V., Giger, S., Roch, A., Auwerx, J. H., & Lütolf, M. P. (2016) · Nature Communications · doi:10.1038/ncomms13125 · Cited by 272 · see citing works
Jin Bing, P. A. N., Li, D., Xu, Y., Zhang, J., Wang, Y., Chen, M., Lin, S., Huang, L., Chung, E. J., Citrin, D. E., et al. (2017) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2017.02.216 · Cited by 244 · see citing works
Kit Regulates HSC Engraftment across the Human-Mouse Species Barrier
Cosgun, K. N., Rahmig, S., Mende, N., Reinke, S., Hauber, I., Schäfer, C., Petzold, A., Weisbach, H., Heidkamp, G. F., Purbojo, A., et al. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.06.001 · Cited by 186 · see citing works
Shao, L., Feng, W., Li, H., Gardner, D., Luo, Y., Wang, Y., Liu, L., Meng, A., Sharpless, N. E., & Zhou, D. (2014) · Blood · doi:10.1182/blood-2013-07-515619 · Cited by 165 · see citing works
Ionizing radiation-induced cellular senescence promotes tissue fibrosis after radiotherapy. A review
Nguyen, H. Q., To, N. H., Zadigue, P., Kerbrat, S., TAILLE, A. D. L., Gouvello, S. L., & Belkacémi, Y. (2018) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2018.06.012 · Cited by 128 · see citing works
The Prolonged Gastrointestinal Syndrome in Rhesus Macaques
MacVittie, T. J., Bennett, A. W., Booth, C. E., Garofalo, M. C., Tudor, G. L., Ward, A. A., Shea‐Donohue, T., Gelfond, D., McFarland, E., Jackson, W., et al. (2012) · Health Physics · doi:10.1097/hp.0b013e318266eb4c · Cited by 119 · see citing works
Senescence drives immunotherapy resistance by inducing an immunosuppressive tumor microenvironment
Maggiorani, D., Lê, O., Lisi, V., Landais, S., Moquin‐Beaudry, G., Lavallée, V., Decaluwe, H., & Beausejour, C. M. (2024) · Nature Communications · doi:10.1038/s41467-024-46769-9 · Cited by 129 · see citing works
Single-Limb Irradiation Induces Local and Systemic Bone Loss in a Murine Model
Wright, L. E., Buijs, J. T., Kim, H., Coats, L. E., Scheidler, A. M., John, S. K., She, Y., Murthy, S., Ma, N., Chin-Sinex, H., et al. (2015) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2458 · Cited by 108 · see citing works
Nicolay, N. H., Perez, R. L., Saffrich, R., & Huber, P. E. (2015) · Oncotarget · doi:10.18632/oncotarget.4358 · Cited by 96 · see citing works
Hematopoietic stem cell senescence and cancer therapy-induced long-term bone marrow injury.
Shao, L., Wang, Y., Chang, J., Luo, Y., Meng, A., & Zhou, D. (2013) · PubMed · doi:10.3978/j.issn.2218-676x.2013.07.03 · Cited by 79 · see citing works
Sehl, M. E., Carroll, J., Horvath, S., & Bower, J. E. (2020) · npj Breast Cancer · doi:10.1038/s41523-020-0161-3 · Cited by 77 · see citing works
Insights into ionizing radiation-induced bone marrow hematopoietic stem cell injury
Zhang, Y., Chen, X., Wang, X., Chen, J., Du, C., Wang, J., & Liao, W. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-03853-7 · Cited by 73 · see citing works
Mesenchymal stromal cells: radio‐resistant members of the bone marrow
Sugrue, T., Lowndes, N. F., & Ceredig, R. (2012) · Immunology and Cell Biology · doi:10.1038/icb.2012.61 · Cited by 56 · see citing works
Restored immune cell functions upon clearance of senescence in the irradiated splenic environment
Palacio, L., Goyer, M., Maggiorani, D., Espinosa, A., Villeneuve, N., Bourbonnais, S., Moquin‐Beaudry, G., Le, O., Demaria, M., Davalos, A. R., et al. (2019) · Aging Cell · doi:10.1111/acel.12971 · Cited by 54 · see citing works
Potential role of senescence in radiation-induced damage of the aged skeleton
Chandra, A., Park, S. S., & Pignolo, R. J. (2018) · Bone · doi:10.1016/j.bone.2018.12.006 · Cited by 53 · see citing works
Despars, G., Carbonneau, C. L., Bardeau, P., Coutu, D. L., & Beausejour, C. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073206 · Cited by 48 · see citing works
Self-citationHuman mesenchymal stem cells lose their functional properties after paclitaxel treatment
Münz, F., Perez, R. L., Trinh, T., Sisombath, S., Weber, K., Wuchter, P., Debus, J., Saffrich, R., Huber, P. E., & Nicolay, N. H. (2018) · Scientific Reports · doi:10.1038/s41598-017-18862-1 · Cited by 48 · see citing works
Frescas, D., Hall, B. M., Strom, E., Virtuoso, L. P., Gupta, M., Gleiberman, A. S., Rydkina, E., Balan, V., Vujcic, S., Chernova, O. B., et al. (2017) · Cell Cycle · doi:10.1080/15384101.2017.1339850 · Cited by 34 · see citing works
Li, Y., Xue, Z., Dong, X., Liu, Q., Liu, Z., Li, H., Xing, H., Xu, Y., Tang, K., Tian, Z., et al. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.11.007 · Cited by 31 · see citing works
Leonard, A. K., Yapundich, M., Nassehi, T., Gamer, J., Drysdale, C. M., Haro‐Mora, J. J., Demirci, S., Hsieh, M. M., Uchida, N., & Tisdale, J. F. (2019) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2019.10.017 · Cited by 30 · see citing works
Qi, Y., Chen, S., Lu, Y., Zhang, Z., Wang, S., Chen, N., Shen, M., Chen, F., Chen, M., Quan, Y., et al. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.08.010 · Cited by 26 · see citing works
Xu, X., Li, R., Zhou, Y., Zou, Q., Ding, Q., Wang, J., Wei-fang, J., Hua, G., & Jianjun, G. (2017) · Stem Cell Research & Therapy · doi:10.1186/s13287-017-0527-0 · Cited by 26 · see citing works
Senescence and Aging: Does It Impact Cancer Immunotherapies?
Maggiorani, D., & Beausejour, C. M. (2021) · Cells · doi:10.3390/cells10071568 · Cited by 23 · see citing works
Zhang, J., Han, X., Zhao, Y., Xue, X., & Fan, S. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.12.021 · Cited by 19 · see citing works
Ripk3 signaling regulates HSCs during stress and represses radiation-induced leukemia in mice
Zhang, L., Luo, H., Ni, H., Liu, S., Xing, H., Zhang, J., Sellin, M., Breslin, P., Wei, W., Denning, M. F., et al. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.04.009 · Cited by 17 · see citing works
Sivananthan, A., Shields, D. S., Fisher, R., Hou, W., Zhang, X., Franicola, D., Epperly, M. W., Wipf, P., & Greenberger, J. S. (2018) · Radiation Research · doi:10.1667/rr15199.1 · Cited by 17 · see citing works
Kojic Acid Protects C57BL/6 Mice from Gamma-irradiation Induced Damage
Wang, K., Liu, C., Di, C., Ma, C., Han, C.-G., Yuan, M., Li, P., Li, L., & Liu, Y.-X. (2014) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2014.15.1.291 · Cited by 14 · see citing works
Chen, X., Chen, L., Tan, J., Zhang, L., Xia, J., Cheng, B., & Zhang, W. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.30051 · Cited by 13 · see citing works
Cell-based immunomodulatory therapy approaches for type 1 diabetes mellitus
Black, L. A., & Zorina, T. D. (2019) · Drug Discovery Today · doi:10.1016/j.drudis.2019.11.016 · Cited by 12 · see citing works
Wang, G. Y., Wood, C. N., Dolorito, J., Libove, E., & Epstein, E. H. (2017) · Oncogene · doi:10.1038/onc.2017.12 · Cited by 11 · see citing works
Immunosenescence: Molecular Mechanisms, Diseases, and Therapeutic Innovations
Gong, N., Pan, X., Deng, Y., Che, J., Bao, J., Wang, M., Xu, C., Liu, X., & Shi, Y. (2025) · MedComm · doi:10.1002/mco2.70515 · Cited by 12 · see citing works
Particle Radiation-Induced Nontargeted Effects in Bone-Marrow-Derived Endothelial Progenitor Cells
Sasi, S. P., Park, D. S., Muralidharan, S., Wage, J., Kiladjian, A., Onufrak, J., Enderling, H., Yan, X., & Goukassian, D. A. (2015) · Stem Cells International · doi:10.1155/2015/496512 · Cited by 8 · see citing works
Capacity of the medullary cavity of tibia and femur for intra-bone marrow transplantation in mice
Fink, D., Pfeiffenberger, U., Bernthaler, T., Schober, S., Thonhauser, K. E., & Rülicke, T. (2019) · PLoS ONE · doi:10.1371/journal.pone.0224576 · Cited by 9 · see citing works
Humanized Mouse Models for Type 1 Diabetes Including Pancreatic Islet Transplantation
Rahmig, S., Bornstein, S. R., Chavakis, T., Jaeckel, E., & Waskow, C. (2014) · Hormone and Metabolic Research · doi:10.1055/s-0034-1390446 · Cited by 7 · see citing works
Sustained p16INK4a expression is required to prevent IR-induced tumorigenesis in mice
Palacio, L., Krishnan, V., Le, N. L. O., Sharpless, N. E., & Beausejour, C. M. (2016) · Oncogene · doi:10.1038/onc.2016.298 · Cited by 7 · see citing works
Li, G., Liu, X., Du, Q., Gao, M., & An, J. (2015) · Experimental Biology and Medicine · doi:10.1177/1535370215594583 · Cited by 6 · see citing works
All Hematopoietic Stem Cells Engraft in Submyeloablatively Irradiated Mice
Forgáčová, K., Savvulidi, F. G., Šefc, L., Linhartová, J., & Nečas, E. (2013) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2013.02.012 · Cited by 6 · see citing works
Fortin, A., Benabdallah, B., Palacio, L., Carbonneau, C. L., Lê, O., Haddad, É., & Beausejour, C. M. (2012) · Stem Cells and Development · doi:10.1089/scd.2012.0438 · Cited by 5 · see citing works
Self-citationTsuboi, I., Harada, T., Hirabayashi, Y., & Aizawa, S. (2020) · Annals of Hematology · doi:10.1007/s00277-020-04095-2 · Cited by 5 · see citing works
Zorina, T. D. (2020) · Stem Cells and Development · doi:10.1089/scd.2020.0148 · Cited by 5 · see citing works
Radiotherapy‐Induced Osteoporosis
Wright, L. E. (2018) · Primer on the metabolic bone diseases and disorders of mineral metabolism · doi:10.1002/9781119266594.ch102 · Cited by 5 · see citing works
Luo, D., Chen, W., Wang, W., Chen, J., Xu, H., Chen, J., & Wang, Y. (2021) · Translational Cancer Research · doi:10.21037/tcr-20-3035 · Cited by 4 · see citing works
Killer, K., Lê, O., & Beausejour, C. M. (2021) · Radiation Research · doi:10.1667/rade-21-00017.1 · Cited by 4 · see citing works
Tsuboi, I., Harada, T., Hirabayashi, Y., Kanno, J., & Aizawa, S. (2016) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b16-00375 · Cited by 4 · see citing works
Chen, F., Zhang, B., Wang, L., Jia, Y., Zeng, Q., Fan, T., Wang, H., Xiong, M., Lin, Y.-X., Zhou, J., et al. (2025) · Stem Cell Research & Therapy · doi:10.1186/s13287-025-04300-x · Cited by 3 · see citing works
Osteoclasts in osteoradionecrosis: Pathogenic mechanisms and emerging therapies
Li, F., Liu, X., Vandevelde, A.-L., Gao, Y., Dessel, J. V., Sun, Y. Z., & Willaert, R. (2025) · Bone · doi:10.1016/j.bone.2025.117605 · Cited by 3 · see citing works
Sugrue, T., Calvo‐Asensio, I., & Ceredig, R. (2016) · Wiley eBooks · doi:10.1002/9781118907474.ch27 · Cited by 3 · see citing works
van Sas, N. C. F., Rousseau, J., Nguyen, F., Bellec, E., Larrsson, E., Becavin, S., Hindorf, C., Abadie, J., Chouin, N., & Barbet, J. (2014) · Journal of Nuclear Medicine · doi:10.2967/jnumed.113.133330 · Cited by 2 · see citing works
Researching the Adoption and Implementation of Innovative Enterprise Information Systems
Tatnall, A. (2009) · Victoria University Research Repository (Victoria University) · Cited by 2 · see citing works
Stress factor – dependent differences in molecular mechanisms of premature cell senescence
Petrova, N. V., Velichko, A. K., Petrova, N. V., Razin, S. V., & Kantidze, O. L. (2015) · Biopolymers and Cell · doi:10.7124/bc.0008f4 · Cited by 1 · see citing works
Heterotopic bone formation derived from multipotent stromal cells is not inhibited in aged mice
Carbonneau, C. L., Despars, G., Moquin‐Beaudry, G., Benabdallah, B., Bouhanik, S., Dépôt, J., Moreau, A., & Beausejour, C. M. (2014) · Cytotherapy · doi:10.1016/j.jcyt.2014.03.004 · Cited by 1 · see citing works
Self-citationMichikawa, Y. (2013) · Journal of Bone Marrow Research · doi:10.4172/2329-8820.1000101
Wu, T. (2020) · IUScholarWorks (Indiana University) · doi:10.7912/c2/2032
Zorina, T. D., & Black, L. A. (2021) · Springer eBooks · doi:10.1007/978-3-030-77052-5_3
Zorina, T. D., & Black, L. A. (2023) · Springer eBooks · doi:10.1007/978-3-031-25378-2_3
- Authors
- Carbonneau, C. L., Despars, G., Rojas-Sutterlin, S., Fortin, A., Le, O., Hoang, T., & Beauséjour, C. M.
- Affiliations
- Centre Hospitalier Universitaire Sainte-Justine (CA)
- Institut de recherche en immunologie et cancer, Université de Montréal, Montréal, QC
- Centre de recherche du Centre Hospitalier Universitaire Ste-Justine,
- Institute for Research in Immunology and Cancer (CA)
- ORCID
- Hoang, Trang
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2012-01-19
- Volume
- 119
- Issue
- 3
- Pages
- 717-726
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- OpenAlex
- W1985999015
- Cited by
- 59
- References
- 46
- Citations by year
- 2025: 3 · 2024: 2 · 2023: 1 · 2022: 1 · 2021: 6 · 2020: 4 · 2019: 5 · 2018: 6 · 2017: 4 · 2016: 4 · 2015: 7 · 2014: 6 · 2013: 5 · 2012: 4
- FWCI
- 3.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Blood (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research (MOP-102709)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
- Keywords
- ionizing radiation, mesenchymal stem cells, Ink4a/Arf, p16INK4a, p19ARF, cellular senescence, senescence-associated β-galactosidase, bone marrow microenvironment, bone marrow homeostasis, lymphocyte development, hematopoiesis
- MeSH terms
- Animals, Bone Marrow, Cell Differentiation, Female, Hematopoietic Stem Cells, Homeostasis, Mice, Inbred C57BL, Radiation, Ionizing, RNA, Messenger, Blotting, Western, Cellular Senescence, Stromal Cells, Apoptosis, Mice, Knockout, Cyclin-Dependent Kinase Inhibitor p16, ADP-Ribosylation Factor 1, Lymphopoiesis, Cell Proliferation, Mice, Real-Time Polymerase Chain Reaction
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